Standard‐space atlas of the viscoelastic properties of the human brain

Hiscox, Lucy V; McGarry, Matthew; Schwarb, Hillary; Houten, Elijah Van; Pohlig, Ryan T.; Roberts, Neil; Huesmann, Graham R.; Burzyńska, Agnieszka; Sutton, Bradley P.; Hillman, Charles H.; Kramer, Arthur F.; Cohen, Neal J.; Barbey, Aron K.; Paulsen, Keith D.; Johnson, Curtis L.

doi:10.1002/hbm.25192

Cited by 55 publications

(53 citation statements)

References 96 publications

(163 reference statements)

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“…This study presents both absolute and normalized measurements. Because stiffness has been shown to vary with age and sex, normalizing within each subject is even more critical with a more heterogeneous subject population 31,32 …”

Section: Discussionmentioning

confidence: 99%

Robustness of MR Elastography in the Healthy Brain: Repeatability, Reliability, and Effect of Different Reconstruction Methods

Svensson

Arcos

Darwish

et al. 2021

Magnetic Resonance Imaging

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Background Changes in brain stiffness can be an important biomarker for neurological disease. Magnetic resonance elastography (MRE) quantifies tissue stiffness, but the results vary between acquisition and reconstruction methods. Purpose To measure MRE repeatability and estimate the effect of different reconstruction methods and varying data quality on estimated brain stiffness. Study Type Prospective. Subjects Fifteen healthy subjects. Field Strength/Sequence 3T MRI, gradient‐echo elastography sequence with a 50 Hz vibration frequency. Assessment Imaging was performed twice in each subject. Images were reconstructed using a curl‐based and a finite‐element‐model (FEM)‐based method. Stiffness was measured in the whole brain, in white matter, and in four cortical and four deep gray matter regions. Repeatability coefficients (RC), intraclass correlation coefficients (ICC), and coefficients of variation (CV) were calculated. MRE data quality was quantified by the ratio between shear waves and compressional waves. Statistical Tests Median values with range are presented. Reconstruction methods were compared using paired Wilcoxon signed‐rank tests, and Spearman's rank correlation was calculated between MRE data quality and stiffness. Holm–Bonferroni corrections were employed to adjust for multiple comparisons. Results In the whole brain, CV was 4.3% and 3.8% for the curl and the FEM reconstruction, respectively, with 4.0–12.8% for subregions. Whole‐brain ICC was 0.60–0.74, ranging from 0.20 to 0.89 in different regions. RC for the whole brain was 0.14 kPa and 0.17 kPa for the curl and FEM methods, respectively. FEM reconstruction resulted in 39% higher stiffness than the curl reconstruction (P < 0.05). MRE data quality, defined as shear‐compression wave ratio, was higher in peripheral regions than in central regions of the brain (P < 0.05). No significant correlations were observed between MRE data quality and stiffness estimates. Data Conclusion MRE of the human brain is a robust technique in terms of repeatability. Caution is warranted when comparing stiffness values obtained with different techniques. Level of Evidence 1 Technical Efficacy Stage 1

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Section: Discussionmentioning

confidence: 99%

Robustness of MR Elastography in the Healthy Brain: Repeatability, Reliability, and Effect of Different Reconstruction Methods

Svensson

Arcos

Darwish

et al. 2021

Magnetic Resonance Imaging

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Section: Methodsmentioning

confidence: 99%

“…The implementation of brain material heterogeneity in the CAB-20MSym template model was derived from the MRE134 template image ( Hiscox et al, 2020 ). This template was constructed using MRE data from 134 healthy, young adults (18–35 years, 78F/56M) using common MRE acquisition and data processing protocols ( Hiscox et al, 2020 ). To adapt the MRE134 template, originally defined in MNI152 space with 2 mm isotropic voxels, it was first non-linearly registered to the CAB-20MSym template space using ANTs non-linear registration ( Avants et al, 2008 ).…”

Section: Methodsmentioning

confidence: 99%

“…The goal of this study is to calibrate and verify a heterogenous FE brain model by leveraging experimental datasets reporting (1) MRE-derived material properties ( Hiscox et al, 2020 ), (2) high rate, in situ , brain displacements measured from human cadaveric specimens using sonomicrometry ( Alshareef et al, 2020a ), and (3) low rate, in vivo , brain strain measured from human volunteers using tagged magnetic resonance imaging (tMRI; Knutsen et al, 2020 ). Material parameters for the model were developed in three phases.…”

Section: Introductionmentioning

confidence: 99%

“…Material parameters for the model were developed in three phases. First, stiffness data from an MRE template image (average of 134 subjects; Hiscox et al, 2020 ) was used to define the relative stiffness gradient throughout the brain model. Second, the linear stiffness parameter was calibrated using low-displacement cases from the Alshareef et al (2020a) dataset and verified using brain strain data from the in vivo tMRI dataset.…”

Section: Introductionmentioning

confidence: 99%

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Calibration of a Heterogeneous Brain Model Using a Subject-Specific Inverse Finite Element Approach

Giudice

Alshareef

et al. 2021

Front. Bioeng. Biotechnol.

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Central to the investigation of the biomechanics of traumatic brain injury (TBI) and the assessment of injury risk from head impact are finite element (FE) models of the human brain. However, many existing FE human brain models have been developed with simplified representations of the parenchyma, which may limit their applicability as an injury prediction tool. Recent advances in neuroimaging techniques and brain biomechanics provide new and necessary experimental data that can improve the biofidelity of FE brain models. In this study, the CAB-20MSym template model was developed, calibrated, and extensively verified. To implement material heterogeneity, a magnetic resonance elastography (MRE) template image was leveraged to define the relative stiffness gradient of the brain model. A multi-stage inverse FE (iFE) approach was used to calibrate the material parameters that defined the underlying non-linear deviatoric response by minimizing the error between model-predicted brain displacements and experimental displacement data. This process involved calibrating the infinitesimal shear modulus of the material using low-severity, low-deformation impact cases and the material non-linearity using high-severity, high-deformation cases from a dataset of in situ brain displacements obtained from cadaveric specimens. To minimize the geometric discrepancy between the FE models used in the iFE calibration and the cadaveric specimens from which the experimental data were obtained, subject-specific models of these cadaveric brain specimens were developed and used in the calibration process. Finally, the calibrated material parameters were extensively verified using independent brain displacement data from 33 rotational head impacts, spanning multiple loading directions (sagittal, coronal, axial), magnitudes (20–40 rad/s), durations (30–60 ms), and severity. Overall, the heterogeneous CAB-20MSym template model demonstrated good biofidelity with a mean overall CORA score of 0.63 ± 0.06 when compared to in situ brain displacement data. Strains predicted by the calibrated model under non-injurious rotational impacts in human volunteers (N = 6) also demonstrated similar biofidelity compared to in vivo measurements obtained from tagged magnetic resonance imaging studies. In addition to serving as an anatomically accurate model for further investigations of TBI biomechanics, the MRE-based framework for implementing material heterogeneity could serve as a foundation for incorporating subject-specific material properties in future models.

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Differences in Brain Volume in Military Service Members and Veterans After Blast-Related Mild TBI

Dennis,

Rowland,

Esopenko

et al. 2024

JAMA Netw Open

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ImportanceBlast-related mild traumatic brain injuries (TBIs), the “signature injury” of post-9/11 conflicts, are associated with clinically relevant, long-term cognitive, psychological, and behavioral dysfunction and disability; however, the underlying neural mechanisms remain unclear.ObjectiveTo investigate associations between a history of remote blast-related mild TBI and regional brain volume in a sample of US veterans and active duty service members.Design, Setting, and ParticipantsProspective cohort study of US veterans and active duty service members from the Long-Term Impact of Military-Relevant Brain Injury Consortium–Chronic Effects of Neurotrauma Consortium (LIMBIC-CENC), which enrolled more than 1500 participants at 5 sites used in this analysis between 2014 and 2023. Participants were recruited from Veterans Affairs medical centers across the US; 774 veterans and active duty service members of the US military met eligibility criteria for this secondary analysis. Assessment dates were from January 6, 2015, to March 31, 2023; processing and analysis dates were from August 1, 2023, to January 15, 2024.ExposureAll participants had combat exposure, and 82% had 1 or more lifetime mild TBIs with variable injury mechanisms.Main Outcomes and MeasuresRegional brain volume was calculated using tensor-based morphometry on 3-dimensional, T1-weighted magnetic resonance imaging scans; history of TBI, including history of blast-related mild TBI, was assessed by structured clinical interview. Cognitive performance and psychiatric symptoms were assessed with a battery of validated instruments. We hypothesized that regional volume would be smaller in the blast-related mild TBI group and that this would be associated with cognitive performance.ResultsA total of 774 veterans (670 [87%] male; mean [SD] age, 40.1 [9.8] years; 260 [34%] with blast-related TBI) were included in the sample. Individuals with a history of blast-related mild TBI had smaller brain volumes than individuals without a history of blast-related mild TBI (which includes uninjured individuals and those with non–blast-related mild TBI) in several clusters, with the largest centered bilaterally in the superior corona radiata and subcortical gray and white matter (cluster peak Cohen d range, −0.23 to −0.38; mean [SD] Cohen d, 0.28 [0.03]). Additionally, causal mediation analysis revealed that these volume differences significantly mediated the association between blast-related mild TBI and performance on measures of working memory and processing speed.Conclusions and RelevanceIn this cohort study of 774 veterans and active duty service members, robust volume differences associated with blast-related TBI were identified. Furthermore, these volume differences significantly mediated the association between blast-related mild TBI and cognitive function, indicating that this pattern of brain differences may have implications for daily functioning.

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Standard‐space atlas of the viscoelastic properties of the human brain

Cited by 55 publications

References 96 publications

Robustness of MR Elastography in the Healthy Brain: Repeatability, Reliability, and Effect of Different Reconstruction Methods

Robustness of MR Elastography in the Healthy Brain: Repeatability, Reliability, and Effect of Different Reconstruction Methods

Calibration of a Heterogeneous Brain Model Using a Subject-Specific Inverse Finite Element Approach

Differences in Brain Volume in Military Service Members and Veterans After Blast-Related Mild TBI

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